Behavioural responses to environmental hypercapnia in two eusocial species of African mole rats

Abstract

Damaraland and naked mole rat are eusocial mammals that live in crowded burrows in which CO is elevated. These species are thought to be highly tolerant of CO but their behavioural responses to hypercapnia are poorly understood. We hypothesized that Damaraland and naked mole rats would exhibit blunted behavioural responses to hypercapnia and predicted that their activity levels would be unaffected at low to moderate (2-5%) CO but increased at > 7% CO. To test this, we exposed Damaraland and naked mole rats to stepwise increases in environmental CO (0-10%) and measured activity, exploratory behaviour, and body temperature. Surprisingly, we found that both species exhibited no differences in movement velocity, distance travelled, zone transitions (exploration), or body temperature at any level of environmental hypercapnia. Conversely, when carbonic anhydrase was inhibited with acetazolamide (50 mg kg intraperitonially, to increase whole-animal acidosis), exploration was significantly elevated relative to hypercapnic controls in both species at all levels of inhaled CO, and naked mole rat body temperature decreased in > 7% CO. We conclude that both species are largely non-responsive to environmental CO, and that this tolerance may be dependent on bicarbonate buffering at the level of the kidney or within the blood.

Nest Carbon Dioxide Masks GABA-Dependent Seizure Susceptibility in the Naked Mole-Rat

“…Intriguingly, we identified a cysteine variation in this position in the published genome [64] of the Damaraland mole-rat (Fukomys damarensis) (Figure 3), a close relative of the naked mole-rat and the only other eusocial mammal species noted to date. Both naked mole-rats and Damaraland mole-rats have been reported to lack clear behavioral responsiveness to high ambient CO 2 [22] (but see [65]). Naked mole-rats and Damaraland mole-rats are the only mammalian species with a native variant in this position in region encoded by exon 22 of KCC2.…”

“…It is clear, however, from a number of experimental studies that naked mole-rats have adapted to tolerate elevated CO 2 levels. These adaptations include prolonged survival even in extreme hypercapnia [15], the lack of typical behavioral and respiratory responses to elevated ambient CO 2 levels [15,[21][22][23], a decreased CO 2 sensitivity of neuronal gap junctions [24], and an insensitivity to certain acidic stimuli [25][26][27].…”

Post-Translational Deimination of Immunological and Metabolic Protein Markers in Plasma and Extracellular Vesicles of Naked Mole-Rat (Heterocephalus glaber)

“…These findings indicate that naked mole-rats are capable of significant metabolic plasticity within their natural environment. Conversely, naked mole-rats are largely non-responsive to hypercapnia and associated acidity-related pain responses are largely absent [49,50]. Naked mole-rats also have numerous adaptations that are not as obviously linked to their natural habitat, including a remarkable resistance to cancer [51,52], they are the only mammalian thermo-conformer and almost entirely ectothermic for regulation of body temperature [53,54] and they have remarkable longevity [55,56,57,58].…”

Fossorial Damaraland mole rats do not exhibit a blunted hypercapnic ventilatory response

“…Recently, we demonstrated that DMRs do not exhibit behavioural responses to hypercapnia, as shown by a lack of change in exploratory behaviour or increased movement velocity in levels of CO 2 up to nearly double the maximum level recorded in DMR burrows (i.e. 10% CO 2 ) [16]. Therefore, based on what is known regarding the burrows of DMRs, their behavioural responses to inhaled CO 2 , and the physiological responses to hypercapnia of other fossorial species, we hypothesized that DMRs are adapted to environmental hypercapnia and predicted that they would exhibit a blunted HCVR and HCMR to acute hypercapnia.…”